Heterozygosity is unrelated to adult fitness measures in a large, noninbred population of great tits (Parus major)

The extent to which heterozygosity-fitness correlations (HFCs) are expected in wild populations is an important and unresolved question in evolutionary biology, because it relates to our understanding of the genetic architecture of fitness. Here, we report a study of HFCs in a wild, noninbred population of great tits (Parus major), based on a sample comprising 281 individuals typed at 26 markers, resulting in a data set comprising over 5600 genotypes. We regressed pedigree-derived f-score and multilocus genetic diversity against eight life-history traits known to be associated with fitness in this population, including lifetime reproductive success (LRS), as well as several morphological traits under weak selection. We found no evidence for either multilocus or single-locus HFCs for any morphological or fitness trait, and further found no evidence that effect sizes were stronger for those life-history traits more closely associated with reproductive fitness. This result may, in part, be explained by the fact that we found no evidence that our set of 26 markers had any power to infer genome-wide heterozygosity in this population and that marker-derived heterozygosity was uncorrelated with pedigree-derived f-score. Overall, these results emphasize the fact that the often-reported strong HFCs detected in small, inbred populations do not reflect a general phenomenon of increasing individual reproductive fitness with increasing heterozygosity.     

Local heterozygosity-fitness correlations with global positive effects on fitness in threespine stickleback

The complex interactions between genetic diversity and evolution have important implications in many biological areas including conservation, speciation, and mate choice. A common way to study these interactions is to look at heterozygosity-fitness correlations (HFCs). Until recently, HFCs based on noncoding markers were believed to result primarily from global inbreeding effects. However, accumulating theoretical and empirical evidence shows that HFCs may often result from genes being linked to the markers used (local effect). Moreover, local effect HFCs could differ from global inbreeding effects in their direction and occurrence. Consequently, the investigation of the structure and consequences of local HFCs is emerging as a new important goal in evolutionary biology. In this study of a wild threespine stickleback (Gasterosteus aculeatus) population, we first tested the presence of significant positive or negative local effects of heterozygosity at 30 microsatellites loci on five fitness components: survival, mating success, territoriality, length, and body condition. Then, we evaluated the direction and shape of total impact of local HFCs, and estimated the magnitude of the impacts on fitness using regression coefficients and selection differentials. We found that multilocus heterozygosity was not a reliable estimator of individual inbreeding coefficient, which supported the relevance of single-locus based analyses. Highly significant and temporally stable local HFCs were observed. These were mainly positive, but negative effects of heterozygosity were also found. Strong and opposite effects of heterozygosity are probably present in many populations, but may be blurred in HFC analyses looking for global effects only. In this population, both negative and positive HFCs are apparently driving mate preference by females, which is likely to contribute to the maintenance of both additive and nonadditive genetic variance.     

HETEROZYGOSITY-FITNESS CORRELATIONS REVEALED BY NEUTRAL AND CANDIDATE GENE MARKERS IN ROE DEER FROM A LONG-TERM STUDY

Heterozygosity-fitness correlations (HFCs) are increasingly reported but the underlying mechanisms causing HFCs are generally poorly understood. Here, we test for HFCs in roe deer ( Capreolus capreolus ) using 22 neutral microsatellites widely distributed in the genome and four microsatellites in genes that are potentially under selection. Juvenile survival was used as a proxy for individual fitness in a population that has been intensively studied for 30 years in northeastern France. For 222 juveniles, we computed two measures of genetic diversity: individual heterozygosity ( H ), and mean d ² (relatedness of parental genomes). We found a relationship between genetic diversity and fitness both for the 22 neutral markers and two candidate genes: IGF1 (Insulin-like Growth Factor I) and NRAMP (natural resistance-associated macrophage protein). Statistical evidence and the size of genetic effects on juvenile survival were comparable to those reported for early development and cohort variation, suggesting a substantial influence of genetic components on fitness in this roe deer population. For the 22 neutral microsatellites, a correlation with fitness was revealed for mean d ², but not for H , suggesting a possible outbreeding advantage. This heterosis effect could have been favored by introduction of genetically distant (Hungarian) roe deer to the population in recent times and, possibly, by the structuring of the population into distinct clans. The locus-specific correlations with fitness may be driven by growth rate advantages and resistance to diseases known to exist in the studied population. Our analyses of neutral and candidate gene markers both suggest that the observed HFCs are likely mainly due to linkage with dominant or overdominant loci that affect fitness ("local" effect) rather than to a genome-wide relationship with homozygosity due to inbreeding ("general" effect).     

Heterozygosity at neutral and immune loci is not associated with neonatal mortality due to microbial infection in Antarctic fur seals

Numerous studies have reported correlations between the heterozygosity of genetic markers and fitness. These heterozygosity–fitness correlations (HFCs) play a central role in evolutionary and conservation biology, yet their mechanistic basis remains open to debate. For example, fitness associations have been widely reported at both neutral and functional loci, yet few studies have directly compared the two, making it difficult to gauge the relative contributions of genome‐wide inbreeding and specific functional genes to fitness. Here, we compared the effects of neutral and immune gene heterozygosity on death from bacterial infection in Antarctic fur seal (Arctocephalus gazella) pups. We specifically developed a panel of 13 microsatellites from expressed immune genes and genotyped these together with 48 neutral loci in 234 individuals, comprising 39 pups that were classified at necropsy as having most likely died of bacterial infection together with a five times larger matched sample of healthy surviving pups. Identity disequilibrium quantified from the neutral markers was positive and significant, indicative of variance in inbreeding within the study population. However, multilocus heterozygosity did not differ significantly between healthy and infected pups at either class of marker, and little evidence was found for fitness associations at individual loci. These results support a previous study of Antarctic fur seals that found no effects of heterozygosity at nine neutral microsatellites on neonatal survival and thereby help to refine our understanding of how HFCs vary across the life cycle. Given that nonsignificant HFCs are underreported in the literature, we also hope that our study will contribute toward a more balanced understanding of the wider importance of this phenomenon.     

Population demography and heterozygosity–fitness correlations in natural guppy populations: An examination using sexually selected fitness traits

Heterozygosity–fitness correlations (HFCs) have been examined in a wide diversity of contexts, and the results are often used to infer the role of inbreeding in natural populations. Although population demography, reflected in population‐level genetic parameters such as allelic diversity or identity disequilibrium, is expected to play a role in the emergence and detectability of HFCs, direct comparisons of variation in HFCs across many populations of the same species, with different genetic histories, are rare. Here, we examined the relationship between individual microsatellite heterozygosity and a range of sexually selected traits in 660 male guppies from 22 natural populations in Trinidad. Similar to previous studies, observed HFCs were weak overall. However, variation in HFCs among populations was high for some traits (although these variances were not statistically different from zero). Population‐level genetic parameters, specifically genetic diversity levels (number of alleles, observed/expected heterozygosity) and measures of identity disequilibrium (g2 and heterozygosity–heterozygosity correlations), were not associated with variation in population‐level HFCs. This latter result indicates that these metrics do not necessarily provide a reliable predictor of HFC effect sizes across populations. Importantly, diversity and identity disequilibrium statistics were not correlated, providing empirical evidence that these metrics capture different essential characteristics of populations. A complex genetic architecture likely underpins multiple fitness traits, including those associated with male fitness, which may have reduced our ability to detect HFCs in guppy populations. Further advances in this field would benefit from additional research to determine the demographic contexts in which HFCs are most likely to occur.     

Sex-Specific Correlations of Individual Heterozygosity,Parasite Load,and Scalation Asymmetry in a Sexually Dichromatic Lizard

Heterozygosity-fitness correlations (HFCs) provide insights into the genetic bases of individual fitness variation in natural populations. However, despite decades of study, the biological significance of HFCs is still under debate. In this study, we investigated HFCs in a large population of the sexually dimorphic lizard Takydromus viridipunctatus (Lacertidae). Because of the high prevalence of parasitism from trombiculid mites in this lizard, we expect individual fitness (i.e., survival) to decrease with increasing parasite load. Furthermore, because morphological asymmetry is likely to influence individuals'' mobility (i.e., limb asymmetry) and male biting ability during copulation (i.e., head asymmetry) in this species, we also hypothesize that individual fitness should decrease with increasing morphological asymmetry. Although we did not formally test the relationship between morphological asymmetry and fitness in this lizard, we demonstrated that survival decreased with increasing parasite load using a capture-mark-recapture data set. We used a separate sample of 140 lizards to test the correlations between individual heterozygosity (i.e., standardized mean d² and HL based on 10 microsatellite loci) and the two fitness traits (i.e., parasite load and morphological asymmetry). We also evaluated and excluded the possibility that single-locus effects produced spurious HFCs. Our results suggest male-only, negative correlations between individual heterozygosity and parasite load and between individual heterozygosity and asymmetry, suggesting sex-specific, positive HFCs. Male T. viridipunctatus with higher heterozygosity tend to have lower parasite loads (i.e., higher survival) and lower asymmetry, providing a rare example of HFC in reptiles.     

Heterozygosity-fitness correlations of conserved microsatellite markers in Kentish plovers Charadrius alexandrinus

Heterozygosity-fitness correlations (HFCs) are frequently used to examine the relationship between genetic diversity and fitness. Most studies have reported positive HFCs, although there is a strong bias towards investigating HFCs in genetically impoverished populations. We investigated HFCs in a large genetically diverse breeding population of Kentish plovers Charadrius alexandrinus in southern Turkey. This small shorebird exhibits highly variable mating and care systems, and it is becoming an ecological model species to understand breeding system evolution. Using 11 conserved and six anonymous microsatellite markers, we tested whether and how heterozygosity was associated with chick survival, tarsus and body mass growth controlling for nongenetic effects (chick sex, hatching date, length of biparental care and site quality) that influence survival and growth. There was no genome-wide effect of heterozygosity on fitness, and we did not find any significant effects of heterozygosity on growth rates. However, two of the 11 conserved markers displayed an association with offspring survival: one marker showed a positive HFC, whereas the other marker showed a negative HFC. Heterozygosity at three further conserved loci showed significant interaction with nongenetic variables. In contrast, heterozygosity based on anonymous microsatellite loci was not associated with fitness or growth. Markers that were correlated with chick survival were not more likely to be located in exons or introns than other markers that lacked this association.     

Heterozygosity–fitness correlations in blue tit nestlings (<Emphasis Type="Italic">Cyanistis caeruleus</Emphasis>) under contrasting rearing conditions

Understanding the relation between genetic variation and fitness remains a key question in evolutionary biology. Although heterozygosity has been reported to correlate with many fitness-related traits, the strength of the heterozygosity–fitness correlations (HFCs) is usually weak and it is still difficult to assess the generality of these associations in natural populations. It has been suggested that HFCs may become meaningful only under particular environmental conditions. Moreover, existing evidence suggests that HFCs may also differ between sexes. The aim of this study was to investigate correlations between heterozygosity in neutral markers (microsatellites) and fitness-related traits in a natural population of blue tits (Cyanistes caeruleus). Additionally, we tested whether sex and environmental conditions may influence the magnitude and direction of HFCs. We found a positive relationship between heterozygosity and body mass of 14 days post-hatching nestlings, but only among females. Our results suggest that the correlation between heterozygosity and nestling body mass observed among female offspring could be attributed to within-brood effects. We failed to find any evidence that environmental conditions as simulated by brood size manipulation affect HFCs.     

Direct and indirect causal effects of heterozygosity on fitness-related traits in Alpine ibex

Heterozygosity–fitness correlations (HFCs) are a useful tool to investigate the effects of inbreeding in wild populations, but are not informative in distinguishing between direct and indirect effects of heterozygosity on fitness-related traits. We tested HFCs in male Alpine ibex (Capra ibex) in a free-ranging population (which suffered a severe bottleneck at the end of the eighteenth century) and used confirmatory path analysis to disentangle the causal relationships between heterozygosity and fitness-related traits. We tested HFCs in 149 male individuals born between 1985 and 2009. We found that standardized multi-locus heterozygosity (MLH), calculated from 37 microsatellite loci, was related to body mass and horn growth, which are known to be important fitness-related traits, and to faecal egg counts (FECs) of nematode eggs, a proxy of parasite resistance. Then, using confirmatory path analysis, we were able to show that the effect of MLH on horn growth was not direct but mediated by body mass and FEC. HFCs do not necessarily imply direct genetic effects on fitness-related traits, which instead can be mediated by other traits in complex and unexpected ways.     

Heterozygosity–fitness correlations in a wild mammal population: accounting for parental and environmental effects

HFCs (heterozygosity–fitness correlations) measure the direct relationship between an individual's genetic diversity and fitness. The effects of parental heterozygosity and the environment on HFCs are currently under‐researched. We investigated these in a high‐density U.K. population of European badgers (Meles meles), using a multimodel capture–mark–recapture framework and 35 microsatellite loci. We detected interannual variation in first‐year, but not adult, survival probability. Adult females had higher annual survival probabilities than adult males. Cubs with more heterozygous fathers had higher first‐year survival, but only in wetter summers; there was no relationship with individual or maternal heterozygosity. Moist soil conditions enhance badger food supply (earthworms), improving survival. In dryer years, higher indiscriminate mortality rates appear to mask differential heterozygosity‐related survival effects. This paternal interaction was significant in the most supported model; however, the model‐averaged estimate had a relative importance of 0.50 and overlapped zero slightly. First‐year survival probabilities were not correlated with the inbreeding coefficient (f); however, small sample sizes limited the power to detect inbreeding depression. Correlations between individual heterozygosity and inbreeding were weak, in line with published meta‐analyses showing that HFCs tend to be weak. We found support for general rather than local heterozygosity effects on first‐year survival probability, and g2 indicated that our markers had power to detect inbreeding. We emphasize the importance of assessing how environmental stressors can influence the magnitude and direction of HFCs and of considering how parental genetic diversity can affect fitness‐related traits, which could play an important role in the evolution of mate choice.     

Local effects drive heterozygosity–fitness correlations in an outcrossing long-lived tree

Heterozygosity–fitness correlations (HFCs) have been used to understand the complex interactions between inbreeding, genetic diversity and evolution. Although frequently reported for decades, evidence for HFCs was often based on underpowered studies or inappropriate methods, and hence their underlying mechanisms are still under debate. Here, we used 6100 genome-wide single nucleotide polymorphisms (SNPs) to test for general and local effect HFCs in maritime pine (Pinus pinaster Ait.), an iconic Mediterranean forest tree. Survival was used as a fitness proxy, and HFCs were assessed at a four-site common garden under contrasting environmental conditions (total of 16 288 trees). We found no significant correlations between genome-wide heterozygosity and fitness at any location, despite variation in inbreeding explaining a substantial proportion of the total variance for survival. However, four SNPs (including two non-synonymous mutations) were involved in significant associations with survival, in particular in the common gardens with higher environmental stress, as shown by a novel heterozygosity–fitness association test at the species-wide level. Fitness effects of SNPs involved in significant HFCs were stable across maritime pine gene pools naturally growing in distinct environments. These results led us to dismiss the general effect hypothesis and suggested a significant role of heterozygosity in specific candidate genes for increasing fitness in maritime pine. Our study highlights the importance of considering the species evolutionary and demographic history and different spatial scales and testing environments when assessing and interpreting HFCs.     

DOES LINKAGE DISEQUILIBRIUM GENERATE HETEROZYGOSITY‐FITNESS CORRELATIONS IN GREAT REED WARBLERS?

Heterozygosity-fitness correlations (HFCs) at noncoding genetic markers are commonly assumed to reflect fitness effects of heterozygosity at genomewide distributed genes in partially inbred populations. However, in populations with much linkage disequilibrium (LD), HFCs may arise also as a consequence of selection on fitness loci in the local chromosomal vicinity of the markers. Recent data suggest that relatively high levels of LD may prevail in many ecological situations. Consequently, LD may be an important factor, together with partial inbreeding, in causing HFCs in natural populations. In the present study, we evaluate whether LD can generate HFCs in a small and newly founded population of great reed warblers (Acrocephalus arundinaceus). For this purpose dyads of full siblings of which only one individual survived to adult age (i.e., returned to breed at the study area) were scored at 19 microsatellite loci, and at a gene region of hypothesized importance for survival, the major histocompatibility complex (MHC). By examining siblings, we controlled for variation in the inbreeding coefficient and thus excluded genome-wide fitness effects in our analyses. We found that recruited individuals had significantly higher multilocus heterozygosity (MLH), and mean d2 (a microsatellite-specific variable), than their nonrecruited siblings. There was a tendency for the survivors to have a more diverse MHC than the nonsurvivors. Single-locus analyses showed that the strength of the genotype-survival association was especially pronounced at four microsatellite loci. By using genotype data from the entire breeding population, we detected significant LD between five of 162 pairs of microsatellite loci after accounting for multiple tests. Our present finding of a significant within-family multilocus heterozygosity-survival association in a nonequilibrium population supports the view that LD generates HFCs in natural populations.     

Assessment of identity disequilibrium and its relation to empirical heterozygosity fitness correlations: a meta‐analysis

Heterozygosity fitness correlations (HFCs) have frequently been used to detect inbreeding depression, under the assumption that genome‐wide heterozygosity is a good proxy for inbreeding. However, meta‐analyses of the association between fitness measures and individual heterozygosity have shown that often either no correlations are observed or the effect sizes are small. One of the reasons for this may be the absence of variance in inbreeding, a requisite for generating general‐effect HFCs. Recent work has highlighted identity disequilibrium (ID) as a measure that may capture variance in the level of inbreeding within a population; however, no thorough assessment of ID in natural populations has been conducted. In this meta‐analysis, we assess the magnitude of ID (as measured by the g₂ statistic) from 50 previously published HFC studies and its relationship to the observed effect sizes of those studies. We then assess how much power the studies had to detect general‐effect HFCs, and the number of markers that would have been needed to generate a high expected correlation (r² = 0.9) between observed heterozygosity and inbreeding. Across the majority of studies, g₂ values were not significantly different than zero. Despite this, we found that the magnitude of g₂ was associated with the average effect sizes observed in a population, even when point estimates were nonsignificant. These low values of g₂ translated into low expected correlations between heterozygosity and inbreeding and suggest that many more markers than typically used are needed to robustly detect HFCs.     

SELECTION ON OVERDOMINANT GENES MAINTAINS HETEROZYGOSITY ALONG MULTIPLE CHROMOSOMES IN A CLONAL LINEAGE OF HONEY BEE

Correlations between fitness and genome‐wide heterozygosity (heterozygosity‐fitness correlations, HFCs) have been reported across a wide range of taxa. The genetic basis of these correlations is controversial: do they arise from genome‐wide inbreeding (“general effects”) or the “local effects” of overdominant loci acting in linkage disequilibrium with neutral loci? In an asexual thelytokous lineage of the Cape honey bee (Apis mellifera capensis), the effects of inbreeding have been homogenized across the population, making this an ideal system in which to detect overdominant loci, and to make inferences about the importance of overdominance on HFCs in general. Here we investigate the pattern of zygosity along two chromosomes in 42 workers from the clonal Cape honey bee population. On chromosome III (which contains the sex‐locus, a gene that is homozygous‐lethal) and chromosome IV we show that the pattern of zygosity is characterized by loss of heterozygosity in short regions followed by the telomeric restoration of heterozygosity. We infer that at least four selectively overdominant genes maintain heterozygosity on chromosome III and three on chromosome IV via local effects acting on neutral markers in linkage disequilibrium. We conclude that heterozygote advantage and local effects may be more common and evolutionarily significant than is generally appreciated.     

Negative effects of individual heterozygosity on reproductive success in a wild bird population

The evolutionary consequences of individual genetic diversity are frequently studied by assessing heterozygosity–fitness correlations (HFCs). The prevalence of positive and negative HFCs and the predominance of general versus local effects in wild populations are far from understood, partly because comprehensive studies testing for both inbreeding and outbreeding depression are lacking. We studied a genetically diverse population of blue tits in southern Germany using a genome‐wide set of 87 microsatellites to investigate the relationship between proxies of reproductive success and measures of multilocus and single‐locus individual heterozygosity (MLH and SLH). We used complimentary measures of MLH and partitioned markers into functional categories according to their position in the blue tit genome. HFCs based on MLH were consistently negative for functional loci, whereas correlations were rather inconsistent for loci found in nonfunctional areas of the genome. Clutch size was the only reproductive variable showing a general effect. We found evidence for local effects for three measures of reproductive success: arrival date at the breeding site, the probability of breeding at the study site and male reproductive success. For these, we observed consistent, and relatively strong, negative effects at one functional locus. Remarkably, this marker had a similar effect in another blue tit population from Austria (~400 km to the east). We suggest that a genetic local effect on timing of arrival might be responsible for most negative HFCs detected, with carry‐over effects on other reproductive traits. This effect could reflect individual differences in the distance between overwintering areas and breeding sites.     

Growth rate correlates to individual heterozygosity in the European eel, Anguilla anguilla L

Heterozygosity-fitness correlations (HFCs) have been reported in populations of many species. We provide evidence for a positive correlation between genetic variability and growth rate at 12 allozyme loci in a catadromous marine fish species, the European eel (Anguilla anguilla L.). More heterozygous individuals show a significantly higher length and weight increase and an above average condition index in comparison with more homozygous individuals. To a lesser extent, six microsatellite loci show a similar pattern, with positive but not significant correlations between heterozygosity and growth rate. The HFCs observed could be explained by an effect of either direct allozyme over-dominance or associative overdominance. Selection affecting some of the allozyme loci would explain the greater strength of the HFCs found at allozymes in comparison with microsatellites and the lack of correlation between MLH at allozymes and MLH at microsatellites. Associative overdominance (where allozyme loci are merely acting as neutral markers of closely linked fitness loci) might provide an explanation for the HFCs if we consider that allozyme loci have a higher chance than microsatellites to be in linkage disequilibrium with fitness loci.     

Genetic variability is unrelated to growth and parasite infestation in natural populations of the European eel (Anguilla anguilla)

Positive correlations between individual genetic heterozygosity and fitness-related traits (HFCs) have been observed in organisms as diverse as plants, marine bivalves, fish or mammals. HFCs are not universal and the strength and stability of HFCs seem to be variable across species, populations and ages. We analysed the relationship between individual genetic variability and two different estimators of fitness in natural samples of European eel, growth rate (using back-calculated length-at-age 1, 2 and 3) and parasite infestation by the swimbladder nematode Anguillicola crassus . Despite using a large data set of 22 expressed sequence tags-derived microsatellite loci and a large sample size of 346 individuals, no heterozygote advantage was observed in terms of growth rate or parasite load. The lack of association was evidenced by (i) nonsignificant global HFCs, (ii) a Multivariate General Linear Model showing no effect of heterozygosity on fitness components, (iii) single-locus analysis showing a lower number of significant tests than the expected false discovery rate, (iv) sign tests showing only a significant departure from expectations at one component, and, (v) a random distribution of significant single-locus HFCs that was not consistent across fitness components or sampling sites. This contrasts with the positive association observed in farmed eels in a previous study using allozymes, which can be explained by the nature of the markers used, with the allozyme study including many loci involved in metabolic energy pathways, while the expressed sequence tags-linked microsatellites might be located in genes or in the proximity of genes uncoupled with metabolism/growth.     

Heterozygosity at a single locus explains a large proportion of variation in two fitness‐related traits in great tits: a general or a local effect?

In natural populations, mating between relatives can have important fitness consequences due to the negative effects of reduced heterozygosity. Parental level of inbreeding or heterozygosity has been also found to influence the performance of offspring, via direct and indirect parental effects that are independent of the progeny own level of genetic diversity. In this study, we first analysed the effects of parental heterozygosity and relatedness (i.e. an estimate of offspring genetic diversity) on four traits related to offspring viability in great tits (Parus major) using 15 microsatellite markers. Second, we tested whether significant heterozygosity–fitness correlations (HFCs) were due to ‘local’ (i.e. linkage to genes influencing fitness) and/or ‘general’ (genome‐wide heterozygosity) effects. We found a significant negative relationship between parental genetic relatedness and hatching success, and maternal heterozygosity was positively associated with offspring body size. The characteristics of the studied populations (recent admixture, polygynous matings) together with the fact that we found evidence for identity disequilibrium across our set of neutral markers suggest that HFCs may have resulted from genome‐wide inbreeding depression. However, one locus (Ase18) had disproportionately large effects on the observed HFCs: heterozygosity at this locus had significant positive effects on hatching success and offspring size. It suggests that this marker may lie near to a functional locus under selection (i.e. a local effect) or, alternatively, heterozygosity at this locus might be correlated to heterozygosity across the genome due to the extensive ID found in our populations (i.e. a general effect). Collectively, our results lend support to both the general and local effect hypotheses and reinforce the view that HFCs lie on a continuum from inbreeding depression to those strictly due to linkage between marker loci and genes under selection.     

Estimating genome-wide heterozygosity: effects of demographic history and marker type

Heterozygosity–fitness correlations (HFCs) are often used to link individual genetic variation to differences in fitness. However, most studies examining HFCs find weak or no correlations. Here, we derive broad theoretical predictions about how many loci are needed to adequately measure genomic heterozygosity assuming different levels of identity disequilibrium (ID), a proxy for inbreeding. We then evaluate the expected ability to detect HFCs using an empirical data set of 200 microsatellites and 412 single nucleotide polymorphisms (SNPs) genotyped in two populations of bighorn sheep (Ovis canadensis), with different demographic histories. In both populations, heterozygosity was significantly correlated across marker types, although the strength of the correlation was weaker in a native population compared with one founded via translocation and later supplemented with additional individuals. Despite being bi-allelic, SNPs had similar correlations to genome-wide heterozygosity as microsatellites in both populations. For both marker types, this association became stronger and less variable as more markers were considered. Both populations had significant levels of ID; however, estimates were an order of magnitude lower in the native population. As with heterozygosity, SNPs performed similarly to microsatellites, and precision and accuracy of the estimates of ID increased as more loci were considered. Although dependent on the demographic history of the population considered, these results illustrate that genome-wide heterozygosity, and therefore HFCs, are best measured by a large number of markers, a feat now more realistically accomplished with SNPs than microsatellites.     

INBREEDING INFLUENCES WITHIN‐BROOD HETEROZYGOSITY‐FITNESS CORRELATIONS (HFCS) IN AN ISOLATED PASSERINE POPULATION

Molecular estimates of inbreeding may be made using genetic markers such as microsatellites, however the interpretation of resulting heterozygosity‐fitness correlations (HFCs) with respect to inbreeding depression is not straightforward. We investigated the relationship between pedigree‐determined inbreeding coefficients (f) and HFCs in a closely monitored, reintroduced population of Stewart Island robins (Petroica australis rakiura) on Ulva Island, New Zealand. Using a full sibling design, we focused on differences in juvenile survival associated specifically with individual sibling variation in standardized multilocus heterozygosity (SH) when expected f was identical. We found that within broods, siblings with higher SH at microsatellite loci experienced a higher probability of juvenile survival. This effect, however, was detected primarily within broods that experienced inbreeding or when inbreeding had occurred in their pedigree histories (i.e., at the parents’ level). Thus we show, for the first time in a wild population, that the strength of an HFC is partially dependent on the presence of inbreeding events in the recent pedigree history. Our results illustrate the importance of realized effects of inbreeding on genetic variation and fitness and the value of full‐sibling designs for the study of HFCs in the context of small, inbred populations.